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Home , Balkan green lizard, European green lizard, Iberian emerald lizard, Lacerta (genus), Ocellated lizard, Psammodromus

H. S. YILDIRIMHAN, C. R. BURSEY, F. N. ALTUNEL

Turk J Zool 2011; 35(4): 519-535 © TÜBİTAK Research Article doi:10.3906/zoo-0910-1

Helminth parasites of the Balkan green , trilineata Bedriaga 1886, from Bursa,

Hikmet Sami YILDIRIMHAN1,*, Charles Robert BURSEY2, Fayık Naci ALTUNEL1 1Uludağ University, Science and Literature Faculty, Department of Biology, 16059 Bursa - TURKEY 2Department of Biology, Pennsylvania State University, Shenango Campus, Sharon, Pennsylvania 16146, USA

Received: 01.10.2009

Abstract: Th irty-eight Balkan green , Lacerta trilineata, from Turkey were examined for helminths. Th ree of Digenea, Plagiorchis elegans, Pleurogenoides medians, Brachylaemus sp. (metacercaria); 2 species of Cestoda, Oochoristica tuberculata and Mesocestoides sp. (tetrathyridium); and 6 species of Nematoda, Abbreviata abbreviata, Ascarops strongylina (larva in cysts), Falcaustra armenica, Oswaldocruzia fi liformis, Skrjabinelazia hoff manni, Skrjabinodon medinae, were found. Lacerta trilineata represents a new host record for each of the parasite species; Plagiorchis elegans, Brachylaemus sp., Oochoristica tuberculata, Mesocestoides sp., Abbreviata abbreviata, Ascarops strongylina (larva), Falcaustra armenica Skrjabinelazia hoff manni, and Skrjabinodon medinae are reported from Turkey for the fi rst time.

Key words: Digenea, Cestoda, Nematoda, , Lacerta trilineata, Turkey

Bursa (Türkiye) ilinden toplanan İri Yeşil Kertenkele (Lacerta trilineata, Bedriaga 1886)’nin helmint faunası

Özet: 38 iri yeşil kertenkele Bursa’ dan (Türkiye) (Lacerta trilineata) helmintleri incelenmek üzere toplanmıştır. Bulunan türlerin 3’ü Digenea; Plagiorchis elegans, Pleurogenoides medians, Brachylaemus sp. (metacercaria), 2’si Cestoda; Oochoristica tuberculata, Mesocestoides sp. (tetrathyridium), 6’sı Nematoda; Abbreviata abbreviata, Ascarops strongylina (kist içinde larva), Falcaustra armenica, Oswaldocruzia fi liformis, Skrjabinelazia hoff manni, Skrjabinodon medinae grubuna aittir. Lacerta trilineata, her bir parazit türü için yeni konak kaydı olup, bu parazitler iri yeşil kertenkeleden ilk kez rapor edilmiştir. Plagiorchis elegans, Brachylaemus sp., Mesocestoides sp., Abbreviata abbreviata, Ascarops strongylina (larva), Falcaustra armenica, Skrjabinelazia hoff manni, Skrjabinodon medinae türleri Türkiye için yeni kayıttır.

Anahtar sözcükler: Digenea, Cestoda, Nematoda, İri Yeşil Kertenkele, Lacerta trilineata, Bursa, Türkiye

Introduction Caucasus, southwestern Iran, , and to elevations up to 650 m (Baran and Atatur, 1998). To Th e Balkan green lizard, Lacerta trilineata our knowledge, there are no reports of helminths in Bedriaga, 1886 (), is known from the L. trilineata. Th e purpose of this paper is to provide Adriatic Sea coast to the Balkan countries, Turkey, an initial helminth list for L. trilineata. * E-mail: [email protected]

519 Helminth parasites of the Balkan green lizard, İ Bedriaga 1886, from Bursa, Turkey

Materials and methods 1927; Plagiorchis brauni Massino 1927; Plagorochis Th irty-eight specimens of Lacerta trilineata (23 loossi Massino 1927; Plagiorchis massino Petrov males, 15 females, mean snout-vent length = 42 and Tichonoff , 1927; Plagiorchis multiglandularis ± 4 mm, range 35-48 mm) were collected by hand Semenow, 1927; Plagiorchis skrajabini Massino 1927; 1996-1998 at Osmangazi (40°10ʹN, 29°01ʹE, 650 m Plagiorchis uhlworni Massino, 1927; Plagiorchis elevation), Bursa province, Turkey. Lizards were killed potanini Skrjabin, 1928; Plagiorchis eutamiatis Schulz, with an overdose of sodium pentobarbital. Th e body 1932; Plagiorchis casarci Mehra, 1937; Plagiorchis cavity was opened, and the digestive tract removed. ferrigunum Mehra, 1937; Plagiorchis eutamiatis Th e esophagus, stomach, small and large intestine, Zibethicus Vassiliev 1939; Plagiorchis extremus Strom, and lungs were opened and separately examined 1940; Plagiorchis strictus Strom, 1940; Plagiorchis for helminths under a dissecting microscope. fuji Ogata, 1941; Plagiorchis ptschelkini Sobolev, Nematodes were killed in hot saline solution, fi xed 1946; Plagiorchis petrovi Fediushin, 1949; Plagiorchis in 70% ethanol, and mounted in glycerol. Digeneans oscineus Sudarikov, 1950; Plagiorchis castoris Orloff and cestodes were fi xed in 70% ethanol, stained with et Moskalev, 1953; Plagiorchis blatnensis Chalupsky, iron-carmine as described by Georgiev et al. (1986), 1954; Plagirochis raabei Furmaga, 1956; Plagirochis cleared in clove oil, and mounted in Entellan®. stefanski Furmaga, 1956, Plagiorchis muris sensu Helminth identifi cation was based on keys given Prokopic and Genov, 1974; Plagiorchis proximus by Schmidt (1986) and Yamaguti (1961). Helminth sensu Prokopic and Genov, 1974; Plagiorchis cuculi voucher specimens were deposited in the helminth Schaldybin, Anikin, Budkin et Suslova, 1977) collection of Uludağ University Museum of , Prevalence and mean intensity: 1/38 (3%), 1 Bursa, Turkey. Lizard specimens were deposited in individual. the Department of Biology, Uludağ University, Bursa, Temporal distribution: 10 Jun 1996, 1 host with 1. Turkey. Site of infection: Small intestine. Lacerta trilineata Type host and type locality: House sparrow, Passer Bedriaga, 1886 domesticus, Germany (Rudolphi, 1802). Th irty-eight L. trilineata (23 males, 15 females), Additional Turkish records: None. Osmangazi, Turkey (6 collected in June 1996, 3 in May 1997, 1 in August 1997, 3 in May 1998, 7 in June Other reported hosts: Amphibia: yellowbelly 1998, 16 in July 1998, and 2 in October 1998). toad, Bombina variegata, (Prokopic and Krivanec, 1975); pool frog, Pelophylas lessonae, (reported as Rana esculenta, Prokopic and Krivanec, 1975); Results common frog, Rana temporaria, (Capuse, 1971); Plagiorchis elegans Reptilia: , Lacerta agilis, (Shevechenko and Barabashova, 1958; Moravec, 1963; Capuse, (Rudolphi, 1802) Braun, 1902 1971; Lewin, 1992a; Shimalov et al., 2000; Sharpilo (Syn. Fasciola elegans Rudolphi, 1802; Fasciola et al., 2001; Borkovcova and Kopriva, 2004); cirratus Rudolphi, 1802; Distoma colubri natricis , Lacerta viridis, (Capuse, intestinale Rudolphi, 1809; Distoma elegans 1971); , Zootoca vivipara, (reported (Rudolphi, 1802) Rudolphi,1809; Distoma colubri as Lacerta vivipara, Lewin, 1992b; Shimalov et al., tesssellati Rudolphi, 1819; Distoma lacertae Rudolphi, 2000); European grass snake, Natrix natrix (Capuse, 1819; Distomum (Brachylaimus) elegans (Rudolphi, 1971); Aves: , Accipiter gentilis, 1802) Dujardin 1845; Distomum erraticum Linstow (Sitko, 1998); Eurasian sparrowhawk, Accipiter nisus, 1894; Plagiorchis cirratus (Rudolphi, 1802) Lühe, (Sitko, 1998); spotted sandpiper, Actitis macularius, 1899; Plagiorchis mentulatus (Rudolphi 1819) (Didyk et al., 2007); Balkal tean, Anas formosa, Stossich, 1904; Plagiorchis asperus Stossich, 1904; (Bykhovskaya-Pavlovskaya, 1962); mallard, Anas Plagiorchis notabilis Nicoll, 1909; Plagiorchis marii platyrhynchos, (Styczynska-Jurewicz, 1962); little Skrajabin, 1920; Plagiorchis blumbergi Massino stint, Calidris minuta, (Bykhovskaya-Pavlovskaya,

520 H. S. YILDIRIMHAN, C. R. BURSEY, F. N. ALTUNEL

1962); twite, Carduelis fl avirostris, (Massino, 1929); Jurewicz, 1962); Eurasian curlew, Numenius arquata, ruddy shelduck, Casarca ferruginea, (Mehra, 1937); (Bykhovskaya-Pavlovskaya, 1962); slender-billed black tern, Chlidonias nigra, (Massino, 1929); western curlew, Numenius tenuirostris, (Bykhovskaya- marsh harrier, Circus aeruginosus, (Bykhovskaya- Pavlovskaya, 1962); tuft ed duck, Nyroca fuligula, Pavlovskaya, 1953; Krasnolobova, 1987); northern (Styczynska-Jurewicz, 1962); Eurasian golden harrier, Circus cyaneus, (Krasnolobova, 1987); oriole, Oriolus oriolus, (Bykhovskaya-Pavlovskaya, pallid harrier, Circus macrourus, (Bykhovskaya- 1962); Eurasia scops owl, Otus scops, (Braun, 1902); Pavlovskaya, 1953; Krasnolobova, 1987); common osprey, Pandion haliaetus, (Krasnolobova, 1987); quail, Coturnix coturnix, (Bykhovskaya-Pavlovskaya , bearded reeding, Panurus biarmicus (Bykhovskaya- 1953); common raven, Corvus corax, (Massino, 1927); Pavlovskaya, 1962); great tit, Parus major, carrion crow, Corvus corone, (Mühling, 1896); rook, (Braun, 1902; Bykhovskaya-Pavlovskaya, 1962); Corvus frugilegus, (Braun, 1902); Eurasian jackdaw, house sparrow, Passer domesticus, (Braun, 1902); Corvus monedula, (Massino, 1927); corncrake, Eurasian sparrow, Passer montanus, (Bykhovskaya- Crex crex, (Macko, 1969); common cuckoo, Pavlovskaya, 1962); coal tit, Periparus ater, (Massino, Cucullus canorus, (Dubinia and Kulakova, 1960); 1929); honey buzzard, Pernis apivorus, (Ferrer et al., common house-martin, Delichon urbica, (Odening, 2004); ruff , Philomachus pugnax, (Bykhovskaya- 1961); great spotted woodpecker, Dendrocopos Pavlovskaya, 1962); black-billed magpie, Pica major, (Styczynska-Jurewicz, 1962); merlin, Falco pica, (Braun, 1902); glossy ibis, Plegadis falcinellus, columbarius, (Massino, 1927; Krasnolobova, 1987); (Bykhovskaya-Pavlovskaya, 1962); dunnock, peregrine falcon, Falco peregrinus, (Krasnolobova, Prunella modularis, (Styczynska-Jurewicz, 1962); 1987); Eurasian hobby, Falco subbuteo, (Bykhovskaya- Eurasian nuthatch, Sitta europaea, (Styczynska- Pavlovskaya, 1953; Styczynska-Jurewicz, 1962; Jurewicz, 1962); common tern, Sterna hirundo, Krasnolobova, 1987; Ferrer et al., 2004); Eurasian (Bykhovskaya-Pavlovskaya, 1962); common starling, kestrel, Falco tinnunculus, (Sitko, 1998); red-footed Sturnus vulgaris, (Bykhovskaya-Pavlovskaya, 1953); falcon, Falco vespertinus, (Styczynska-Jurewicz, barred warbler, Sylvia nisoria, (Bykhovskaya- 1962; Krasnolobova, 1987); common chaffi nch, Pavlovskaya, 1962); hazel grouse, Tetrastes bonasia, Fringilla coelebs, (Bykhovskaya-Pavlovskaya , 1962); (Bykhovskaya-Pavlovskaya, 1962); wood sandpiper, common snipe, Gallinago gallinago, (Massino, 1927); Tringa glareola, (Bykhovskaya-Pavlovskaya, 1962); chicken, Gallus gallus domesticus, (Odening, 1959); fi eldfare, Turdus pilaris (Bykhovskaya-Pavlovskaya, Eurasian jay, Garrulus glandarius, (Bykhovskaya- 1962); hoopoe, Upupa epops, (Bykhovskaya- Pavlovskaya, 1953); collared pratincole, Glareola Pavlovskaya, 1962); Mammalia: arctic fox, Alopex pratincola, (Braun, 1902; Bykhovskaya-Pavlovskaya, lagopus, (Malczewski, 1961; Rausch et al., 1983); 1962); barn swallow, Hirundo rustica, (Odening, striped fi eld mouse, Apodemus agrarius, (Furmaga, 1961); red-backed shrike, Lanius collurio, (Massino, 1956; Zarnowski, 1960; Shimalov, 2002); yellow- 1927); herring gull, Larus argentatus, (Bykhovskaya- necked mouse, Apodemus fl avicollis, (Matskasi, Pavlovskaya, 1962); great black-headed gull, Larus 1971); wood mouse, Apodemus sylvaticus, (Furmaga, ichthyaetus, (Mhaisen et al., 1990); common black- 1956); dog, Canis familiaris, (Petrov and Tichonoff , headed gull, Larus ridibundus, (Bykhovskaya- 1927; Desrochers and Curtis, 1987); bank vole, Pavlovskaya, 1962); Hudsonian godwit, Limosa Clethrionomys glareolus, (Matskasi, 1971; Tenora et haemastica (Kinsella et al., 2007); black-tailed godwit, al., 1983; Mazeika et al., 2003); cat, Felis domesticus, Limosa limosa, (Bykhovskaya-Pavlovskaya, 1962); (Petrov and Tichonoff , 1927); harvest mouse, Eurasian black grouse, Lyrurus tetrix, (Bykhovskaya- Micromys minutus, (Matskasi, 1971); common Pavlovskaya, 1962); Eurasian swift , Micropus vole, Microtus arvalis, (Chalupsky, 1954); house apus, (Odening, 1961); black kite Milvus migrans, mouse, Mus musculus, (Odening, 1959); water (Krasnolobova, 1987); white wagtail, Motacilla alba, shrew, Neomys fodiens, (Panov and Karpenko, 2004); (Bykhovskaya-Pavlovskaya, 1962); yellow wagtail, muskrat, Ondatra ziabethicus, (Sey, 1965; Matskasi, Motacilla fl ava, (Bykhovskaya-Pavlovskaya, 1962); 1971); common shrew, Sorex araneus, (Matskasi, spotted fl ycatcher, Muscicapa striata, (Styczynska- 1971).

521 Helminth parasites of the Balkan green lizard, İ Bedriaga 1886, from Bursa, Turkey

Geographic range: Northern hemisphere. Nabelkova, 1964; Kozak, 1973); agile frog, Rana Remarks: All species of Plagiorchis use aquatic dalmatina, (Kozak, 1973; Prokopic and Krivanec, snails as fi rst intermediate hosts and as second 1975); Rana temporaria (Kopriva, 1957; Vojtkova intermediate hosts (Roberts and Janovy, 2000). and Krivanec, 1970; Prokopic and Krivanec, 1975; Given the broad host-range any insectivore might Cedhagen, 1988; reported as Rana platyrrhinus, be expected to harbor Plagiorchis elegans. Lacerta Bovien, 1916;); common newt, Lissotrition vulgaris, trilineata represents a new host record for P. elegans; (reported as Triturus vulgaris, Vojtkova, 1963; Turkey is a new locality record. Vojtkova and Vojtek, 1972); northern crested newt, Triturus cristatus, (Vojtkova, 1963; Vojtkova and Pleurogenoides medians (Olsson, 1876) Vojtek, 1972); Reptilia: Lacerta agilis, (Lewin, 1992a; Travassos, 1921 Sharpilo et al., 2001); Iberian wall lizard, (Syn. Distomum medians Olsson, 1876) hispanica, (Roca et al, 1986a; Roca and Lluch, 1988). Prevalence, mean intensity, and range: 2 of 38 Geographic range: Western Palaearctic. (5%), 3.0 ± 2.8, 1-5. Remarks: Lacerta trilineata represents a new host Temporal distribution: 13 August 1997, 1 host with record for P. me di an s . 5; 4 June 1998, 1 host with 1. Brachylaemus sp. (metacercariae) Site of infection: Small intestine. Prevalence, mean intensity, and range: 3 of 38 Type host and type locality: common European (9%), 5.0 ± 6.9, 1-13. toad, Bufo bufo, Sweden (reported as Bufo vulgaris, Temporal distribution: 22 May 1997, 1 host with Olsson, 1876). 1; 4 June 1998, 1 host with 13; 24 June 1998, 1 host Additional Turkish records: European treefrog, with 1. Hyla arborea, (Dusen and Oz, 2004); marsh Site of infection: Small intestine. frog, Pelophylax ridibundus, (reported as Rana Additional Turkish records: None. ridibunda, Yıldırımhan et al., 1996; Yıldırımhan et al., 2005; Düşen and Öz, 2006; Saglam and Arikan, Other reported hosts (metacercaria in Reptilia 2006); Caucasian brown frog, Rana macrocnemis, only): Reptilia: Slow worm, Anguis fragilis, (Lewin, (Yıldırımhan et al., 2006, reported as Rana camerani, 1990); Lacerta agilis, (Lewin, 1992a); Bocage’s wall Düşen, 2007). lizard, Podarcis bocagei, (Roca et al, 1989); Carbonell’s wall lizard, Podarcis carbonelli, (Galdón et al., 2006); Other reports: Amphibia: European fi re-bellied Lilford’s wall lizard, Podarcis lilfordi, (Hornero and toad, Bombina bombina, (Vojtkova, 1961; Vojtkova et Roca, 1992b: Roca and Hornero, 1994); Ibiza wall al., 1963; Kozak, 1973); Bufo bufo, (Volna-Nabelkova, lizard, Podarcis pityusensis, (Roca and Hornero, 1964; Cox, 1971; Kozak, 1973; Fernandez et al., 1994). 1986; Shimalov and Shimalov, 2001); Hyla arborea, (Volna-Nabelkova, 1964; Kozak, 1969, 1973); Geographic range: For metacercaria in : Pelophylax lessonae, (reported as Rana esculenta, Poland (Lewin, 1990); (Galdon et al., 2006); André, 1913; Bovien, 1916; Kopriva, 1957; Vojtkova, (Roca et al., 1989); Turkey (this report). 1961; Vojtkova et al., 1963; Volna-Nabelkova, Remarks: In the life cycle of Brachylaemus spp., 1964; Kozak, 1966, 1968, 1969, 1973; Combes et terrestrial gastropods and rodents are intermediate and al., 1973; Prokopic and Krivanec, 1975; Kuc and defi nite hosts, respectively (Gracenea and González- Sulgostowska, 1988a; Popovic and Mikes, 1989); Moreno, 2002). Th e presence of Brachylaemus Pelophylax ridibundus, (reported as Rana ridibunda, in lizards is considered atypical, probably due to Buchvarov, 1962; Combes and Gerbeaux, 1970; Cox, ingestion of snails harboring this trematode (Galdón 1971; Kozak, 1973; Kuc and Sulgostowska, 1988b; et al., 2006). Lacerta trilineata represents a new Popovic and Mikes, 1989; Saeed et al., 2007); green host record for the Brachylaemus. However, toad, Pseudepidalea viridis, (reported as Bufo viridis, this occurrence should be considered as accidental Kolendo, 1959); moor frog, Rana arvalis, (Volna- parasitism. Turkey is a new locality record.

522 H. S. YILDIRIMHAN, C. R. BURSEY, F. N. ALTUNEL

Oochoristica tuberculata Psammmodromus algirus, (Della Santa, 1956); Spanish (Rudolphi, 1819) Lühe, 1898 , , (Della Santa, 1956; Roca et al., 1986b; Roca and Lluch, 1988); (Syn. Taenia tuberculata Rudolphi, 1819; Taenia European glass lizard, Pseudopus apodus, (Della rotundata Molin, 1859; Taenia pseudopodis Krabbe, Santa, 1956; Vakker et al., 1985); sandfi sh skink, 1879; Taenia truncata Krabbe, 1879, in part; Scincus scincus, (Groschaft and Moravaec, 1983); Oochroistica rotundata [Molin, 1859] Parona, 1900; Tenerife wall gecko, Tarentola delalandii, (Roca et al., Oochoristica pseudopodis [Krabbe, 1879] Zschokke, 1987); common wonder gecko, Teratoscincus scincus, 1905; Oochoristica truncata [Krabbe, 1879] (Markov and Paraskiv, 1956); steppe agama, Trapelus Zschokke, 1905, in part; Oochoristica indica Misra, sanguinolenta, (Della Santa, 1956); North African 1945; Oochoristica agamae Baylis, 1919 sensu Roca mastigure, Uromastyx acanthinura, (Della Santa, et al., 1986). 1956; Dupouy and Kehemir, 1973); desert monitor, Prevalence, mean intensity, and range: 6 of 38 Varanus griseus, (Della Santa, 1956); Sahara sand (16%), 6.5 ± 4.5, 1-11. viper, Cerastes vipera, (Dollfus, 1932); Montpellier Temporal distribution: 4 May 1998, 2 hosts with snake, Malpolon monspessulanus, (Joyeux and Gaud, 1, 7, respectively; 3 June 1998, 1 host with 9; 24 June 1945; Della Santa, 1956; Dupouy and Kechemir, 1998, 1 host with 10; 25 June 1998, 1 host with 11; 7 1973); striped sand snake, Psammophis sibilans, July 1998, 1 host with 1. (Joyeux and Baer, 1928). Site of infection: Small intestine. Geographic range: Palaearctic (Della Santa, 1956). Type host and type locality: , Remarks: Oochoristica, a cosmopolitan genus of lepidus, Spain (=Lacerta lepida, Rudolphi, 1819). cestodes parasitic in lizards, snakes, and turtles, was erected by Lühe (1898) to receive a revision of the Additional Turkish records: Caucasian agama, cestode, Taenia tuberculata, originally described by Laudakia caucasia, (Yıldırımhan et al., 2006). Rudolphi (1819). Since then, over 65 species have Other reported hosts: Reptilia: fringe-fi ngered been assigned to the genus (see Schmidt, 1986). lizard, Acanthodactylus erythrurus, (Dollfus, 1958; Several of these species have been shown to exhibit Busack and Jaksic, 1982; Roca et al., 1986b; Roca and marked similarity and synonymy has oft en been Lluch, 1988); rainbow lizard, Agama agama, (Joyeux proposed. For example, Baer (1927) considered and Baer, 1928; Della Santa, 1956); eastern garden Taenia (= Oochoristica) truncata Krabbe, 1879 to lizard, Calotes versicolor, (Misra, 1945); ocellated be a synonym of O. tuberculata Dollfus (1932) and skink, Chalcides ocellatus, (Lühe, 1898; Parona, 1887, Hughes (1940) also advocated synonymy. However, 1900; Barbagallo, 1901; Rizzo, 1902; Mingazzini, Spasskii (1951) considered geographic distribution 1904; Della Santa, 1956; Groschaft and Moravec, (western Palaearctic vs. Africa) suffi cient to separate 1983; Ibrahim et al., 2005); Gran Canaria skink, the 2 species and did not accept the synonymy but Chalcides sexlineatus, (Lamas et al., 1985); Canarian did synonymize Oochoristica agamae Baylis, 1919; cylindrical skink, Chalcides viridanus, (Roca et al., Oochoristica africana Malan, 1939; and Oochoristica 1987); Schneider’s skink, Eumeces schneideri, (Baer, africana var. ookispensis Malan, 1939 with O. truncata. 1928); keeled Indian mabuya, Eutropis carinata, Raina et al. (1975) in their report of cestodes from (Della Santa, 1956); Lacerta agilis, (Ivanitsky, 1940; Agama tuberculata collected in Kashmir discuss Della Santa, 1956; Shevechenko and Barabashova, the diffi culty of assigning their specimens to O. 1958; Sharpilo et al., 2001; Mihalca et al., 2007); truncata or O. tuberculata and aft er comparing Lacerta viridis, (Della Santa, 1956); Kashmir rock structural attributes of the 2 species concluded that agama, Laudakia tuberculata, (Raina et al., 1975); O. truncata is a synonym of O. tuberculata. We refer common wall lizard, , (Cerutti, all published Palaearctic occurrences of O. truncata 1902; Joyeux and Baer, 1936; Lopez-Neyra, 1944; to O. tuberculata and retain, at least temporarily, sub- Della Santa, 1956); Algerian psammmodromus, Sarahian occurrences as O. truncata.

523 Helminth parasites of the Balkan green lizard, İ Bedriaga 1886, from Bursa, Turkey

Mesocestoides sp. (tetrathyridium) Other reports: Reptilia: Lacerta agilis, (Goldin, Prevalence,and intensity: 1 of 38 (3%), 80. 1975); Lacerta schreiberi, (Roca and Ferragut, 1989); Algerian ocellated lizard, Timon pater, (Seurat, 1917); Temporal distribution: 10 June 1996, 1 host with Dolichophis jugularis, (reported as Coluber jugularis, 80. Biserkov, 1995); Natrix natrix, (Kirin, 2002b); Site of infection: Body cavity. Platyceps najadum, (reported as Coluber najadum, Additional Turkish records: None. Biserkov, 1995); Vipera ammodytes, (Biserkov, 1995). Other reported hosts: Reptilia: Anguis fragilis Geographic range: Algeria (Seurat, 1917); (Lewin, 1990); Lacerta agilis (Lewin, 1992a; Sharpilo (Biserkov, 1995); Crimea (Goldin, 1975); Spain (Roca et al., 2001); , Lacerta schreiberi, and Ferragut, 1989); Turkey (this report). (Roca and Ferragut, 1989); Lacerta viridis, (Biserkov and Kostadinova, 1980); secret toadhead agama, Remarks: Lacerta trilineata represents a new host Phrynocephalus mystaceus, (Ikromov and Cho, record for A. abbreviata; Turkey is a new locality 2004); Podarcis bocagei, (Roca et al., 1989); Podarcis record. hispanica, (Roca et al., 1989); Podarcis muralis, Ascarops strongylina (Kirin, 2002a); Podarcis pityusensis, (Roca and (Rudolphi, 1819) Alicata and McIntosh, 1933 Hornero, 1994); Psammodromus hispanicus, (Roca et al., 1986b; Roca and Lluch, 1988); smooth snake, (larvae in cysts) Coronella austriaca, (Biserkov, 1996); Aesculapean (Syn. Spiroptera strongylina Rudolphi, 1819). snake, Zamenis longissimus (reported as Elaphe longissima, Biserkov, 1996); Haly’s pit viper, Glodius Prevalence and intensity: 1 of 38 (3%), 7. halys, (reported as Ancystrodon halys, Bogdanov et Temporal distribution: 10 July 1998, 1 host with 7. al., 1969); Natrix natrix, (Lewin, 1992b). Site of infection: cysts on stomach wall. Geographic range: Cosmopolitan (McAllister et Type host and type locality: Mammal, pig, Sus al., 1991). scrofa, (Rudolphi, 1819). Remarks: Th e life cycle of Mesocestoides spp. is Additional Turkish records: None thought to require 3 hosts, i.e. a vertebrate defi nite host, a vertebrate second intermediate host, and a Other reports: Amphibia: Bufo viridis, (Vashetko purported arthropod fi rst intermediate host (Rausch, and Siddikov, 1999); Reptilia: Anguis fragilis, 1994). Tetrathyrida are frequently found in the body (Shimalov et al., 2000); Lacerta agilis, (Shimalov et cavities of amphibians, reptiles, and rodents (Padgett al., 2000; Sharpilo et al., 2001); Zootoca vivipara, and Boyce, 2004). Lacerta trilineata represents a new (reported as Lacerta vivipara, (Shimalov et al, 2000); host record for the genus Mesocestoides. Turkey is a large whip snake, Dolichophis jugularis, (reported as new locality record. Coluber jugularis, Biserkov, 1995); Dahl’s whip snake, Abbreviata abbreviata Platyceps najadum, (reported as Coluber najadum, (Rudolphi, 1819) Travassos, 1920 Biserkov, 1995); Coronella austriaca, (Shimalov and Shimalov, 2000); Gloydius halys (reported as Prevalence, mean intensity, and range: 1 of 38 Ancystrodon halys, Bogdanov et al., 1969); Malpolon (3%), 15. monspessulanus, (Biserkov, 1995), Natrix natrix, Temporal distribution: 10 June 1996, 1 host with (Shimalov and Shimalov, 2000); Asp viper, Vipera 15. aspis, (Santos et al., 2006); Vipera berus, (Shimalov Site of infection: Stomach. and Simalov, 2000); Lataste’s viper, Vipera latastei Type host and type locality: unknown lizard, Spain (Santos et al., 2006). (Rudolphi, 1819). Geographic range: Cosmopolitan (Yamaguti, Additional Turkish records: None. 1961).

524 H. S. YILDIRIMHAN, C. R. BURSEY, F. N. ALTUNEL

Remarks: Only western Palaearctic records of Prevalence, mean intensity, and range: Hosts larval infections are given here. Larvae in cysts are infected, 2 of 36 (5%), 1.5 ± 0.7, 1-2. frequently found in the body cavities of amphibians, Temporal distribution: 2 July 1998, 2 hosts with 1, reptiles, birds, and mammals (Goldberg and Bursey, 2, respectively. 2000). Lacerta trilineata represents a new host record for larva of Ascrops strongylina. Turkey is a new Site of infection: Small intestine. locality record. Additional Turkish hosts: Square-marked toad, Falcaustra armenica Amietophrynus regularis, (reported as Bufo regularis, Schad et al., 1960); Bufo bufo, (Yıldırımhan and Massino, 1924 Karadeniz, 2007); Pseudepidalea viridis, (reported as (Syn. Spironoura armenica [Massino 1924] Yorke Bufo viridis, Schad et al., 1960; Yıldırımhan, 1999); and Maplestone, 1926). Hyla arborea, (Yıldırımhan, Altunel, et al., 2006); Prevalence and intensity: 1 of 38 (3%), 10. Rana macrocnemis, (Schad et al. 1960; Yıldırımhan et al., 1997; Yıldırımhan, Bursey et al., 2006; reported as Temporal distribution: 10 June 1996, 1 host with Rana camerani, Yıldırımhan, Goldberg et al., 2006); 10. Pelophylax ridibundus (reported as Rana ridibunda, Site of infection: Large intestine. Yıldırımhan, et al., 2005; Sağlam and Arikan, 2006); Type host and type locality: European pond turtle, banded newt, Ommatotriton vittatus, (reported as Emys orbicularis, Armenia (Massino, 1924). Triturus vittatus, Yıldırımhan, 2008); Anguis fragilis, (Schad et al., 1960); Crimean wall lizard, Podarcis Additional Turkish records: Emys orbicularis, tauricus, (reported as Lacerta taurica, Schad et al., (reported as Spironoura armenica, Yıldırımhan and 1960); Lacerta viridis, (Schad et al., 1960). Şahin, 2005); Western Caspian turtle, Mauremys rivulata, (Yıldırımhan et al., 2005). Type host and locality: Rana temporaria, Europe (Goeze, 1782). Other reports: Reptilia: Emys orbicularis, (Ivanitzky, 1940; Hristovski, 1973; Sharpilo, 1976; Other reported hosts: Pisces. chub, Leuciscus Velikanov, 1982, Mihalca et al., 2007); Caspian turtle, cephalus, (Moravec and Scholz, 1991); burbot, Lota Mauremys caspica, (reported as Clemmys caspica, lota, (Novokhatskaya, 2007). Amphibia. Bombina Hristovski, 1973; Sharpilo, 1976; Lees et al., 1985). bombina, (Volna-Nabelkova, 1964; Kozák, 1969, 1973; Moravec and Vojtková, 1975; Prokopic and Geographic range: Central Asia (Sharpilo, 1976); Krivanec, 1975; Rozman, 1976; Vojtková, 1976); (Mihalca et al., 2007); Turkey (Yıldırımhan Bombina variegata, (Prokopic, 1957; Buchvarov, 1962; and Şahin, 2005); Yugoslavia (Hristovski, 1973). Volna-Nabelkova, 1964; Kozák, 1969, 1973; Prokopic Remarks: Lacerta trilineata represents a new host and Krivanec, 1975; Rozman, 1976; Vojtková, 1976; record for F. armenica. Kirin and Buchvarov, 2002a); Bufo bufo, (John, 1957; Oswaldocruzia fi liformis Prokopic, 1957; Kozlowska, 1960; Vojtková, 1961, 1976; Buchvarov, 1962; Vojtková et al, 1963; Volna- (Goeze, 1782) Travassos, 1917 Nabelkova, 1964; Kozák, 1969, 1973; Hristovski and (Syn. Ascaris fi liformis, Goeze, 1782; Cucullanus Riggio, 1971; Schmidt and Enigk, 1972; Canning et ranae Goeze, 1782; Ascaris tennissima Schrank, 1788; al., 1973; Frandsen, 1974; Moravec and Vojtková, Ascaris intestinalis Gmelin, 1790; Ascaris bufonis 1975; Prokopic and Krivanec, 1975; Rozman, 1976; Gmelin, 1790; Strongylus auricularis Zeder, 1800; Ryzhikov et al., 1980; Hendrikx, 1983; Galli et al., Ascaris setiformis Goeze in Zeder, 1800; Strongylus 2001; Shimalov and Shimalov, 2001; reported as Bufo dispar Dujardin, 1845; Oswaldocruzia insulae vulgaris, Baylis, 1928; Travassos, 1937); Himalayan Morishita, 1923; Strongylus bialata Molin, 1861; toad, Duttaphrynus himalayanus (reported as Bufo Oswaldocruzia molgeta Lewis, 1928; Oswaldocruzia himalayanus, Soota and Dey Sarka, 1980); natterjack skrjabini Travassos, 1937; Oswaldocruzia problematica toad, Epidalea calamita (reported as Bufo calamita, Ivanitzky, 1940; Oswaldocruzia goezi Skrjabin and Frandsen, 1974); Euphlyctis cyanophlyctis, (Tandon et Schulz, 1952) al., 2001); Hyla arborea, (Kozlowska, 1960; Vojtková,

525 Helminth parasites of the Balkan green lizard, İ Bedriaga 1886, from Bursa, Turkey

1961, 1976; Volna-Nabelkova, 1964; Kozák, 1969, Moravec and Vojtková, 1975; Prokopic and Krivanec, 1973; Frandsen, 1974; Hristovski and Riggio, 1974; 1975; Rozman, 1976; Vojtková, 1976; Ryzhikov et Prokopic and Krivanec, 1975; Rozman, 1976; al., 1980; Sattmann, 1986; Cedhagen, 1988; Kuc and Ryzhikov et al., 1980); Mediterranean treefrog, Hyla Sulgostowska, 1988a; Griffi n, 1988, 1989; Kirin and meridionalis, (Baker, 1981; Galeano et al., 1990); Buchvarov, 2002a); Sardinia salamander, Atylodes Pelobates fuscus, (Kozlowska, 1960; Kozák, 1969, genei (reported as Speleomantes genei, Ricci, 1987); 1973; Prokopic and Krivanec, 1975; Antsyshkina fi re salamander, Salamandra salamandra, (Barus et et al., 1976; Vojtková, 1976; Ryzhikov et al., 1980); al., 1963; Moravec and Vojtková, 1975; Grabda and Pelophylax lessonae (reported as Rana lessonae, Grabda, 1953; Bertman, 1986); Laurenti’s alpine Borisova, 1988; reported as Rana esculenta, Rozman, newt, Ichthyosaura alpestris (reported as Triturus 1971, 1976; Ryzhikov et al., 1980); Rana macrocnemis, alpestris, Barus and Groschaft , 1962); , (Ryzhikov et al., 1980); marsh frog, Pelophylax Lissotriton helveticus (reported as Molge palmate, ridibundus, (reported as Rana ridibunda , Dubinina, Lewis, 1928; reported as Triturus helveticus, Avery, 1950; Buchvarov, 1962, 1965; Tscherner, 1966; Kozák, 1971); , Lissotrition vulgaris (reported 1969, 1973; Combes and Gerbeauz, 1970; Frandsen, as Molge vulgaris, Baylis, 1928; Lewis, 1928; Hsü 1974; Buchvarov et al., 1975; Prokopic and Krivanec, and Chow, 1938; reported as Triturus vulgaris, 1975; Rozman, 1976; Ryzhikov et al., 1980; Kirin Tranko-Tulecka, 1959; Kozlowska, 1960; Barus and and Buchvarov, 2002b; reported as Rana esculenta, Groschaft , 1962; Vojtková, 1963, 1976; Avery, 1971; Kozlowska, 1960; Vojtková, 1961, 1976; Vojtková Daiya, 1973; Frandsen, 1974; Moravec and Vojtková, et al., 1963; Volna-Nabelkova, 1964; Kozák, 1968; 1975; Ryzikov, et al. 1980); northern crested newt, Plasota, 1969; Messner and Kerstan, 1978; Kuc Triturus cristatus, (Kozlowska, 1960; Frandsen, and Sulgostowska, 1988a); Pseudepidalea viridis 1974; Vojtková, 1976; Bertman, 1994). Reptilia. (reported as Bufo viridis, Kolendo, 1959; Kozlowska, Anguis fragilis, (Sharpilo, 1962, 1976; Moravec, 1960; Volna-Nabelkova, 1964; Buchvarov, 1965; 1963; Bertman and Okulewicz, 1987; Lewin, 1990; Kozák, 1969, 1973; Frandsen, 1974; Hristovski and Shimalov et al., 2000; Borkovcova and Kopriva, Riggio, 1974; Buchvarov et al., 1975; Prokopic and 2005); Lacerta agilis, (Shevechenko and Barabashova, Krivanec, 1975; Vojtková, 1976; Ryzhikov et al., 1980; 1958; Moravec, 1963; Moravec and Vojtková, 1975; Al-Barwari and Nassir, 1983; Vashetko and Siddikov, Okulewicz, 1976; Lewin, 1992b; Shimalov et al., 1999; Rozman, 1976; Shimalov and Shimalov, 2001; 2000; Sharpilo et al., 2001); Lacerta viridis, (Moravec, Saeed et al., 2007); Khabarovsk frog, Rana amurensis, 1963; Marconcini and Triantafi llu, 1970; Moravec (Ryzhikov et al., 1980); moor frog, Rana arvalis, and Vojtková, 1975; Biserkov and Kostadinova, (Prokopic, 1957; Kozlowska, 1960; Vojtková et al, 1963; 1998; Kirin, 2002a; Borkovcova and Kopriva, 2005); Volna-Nabelkova, 1964; Kozák, 1969, 1973; Plasota, armored glass lizard, Pseudopus apodus, (reported 1969; Frandsen, 1974; Prokopic and Krivanec, 1975; as Ophisaurus apodus, Sharpilo, 1976); Amur grass Antsyshkin et al., 1976; Vojtková, 1976; Ryzhikov lizard, Takydromus amurensis, (Sharpilo, 1976); et al., 1980; Borisova, 1988; Cedhagen, 1988; Kuc Zootoca vivipara, (Sanchis et al., 2000; reported as and Sulgostowska, 1988a; Zhigileva, 2007); spring Lacerta vivipara, Travassos, 1937; Moravec, 1963; frog, Rana dalmatina, (Buchvarov, 1962; Volna- Moravec and Vojtková, 1975; Shimalov et al., 2000); Nabelkova, 1964; Kozák, 1969, 1973; Frandsen, 1974; Coronella austriaca, (Sharpilo, 1976); Natrix natrix, Buchvarov et al., 1975; Prokopic and Krivanec, 1975; (Moravec, 1963; Kozák, 1967; Moravec and Vojtková, Vojtková, 1976; Moravec and Scholz, 1991; Kirin and 1975; Bertman and Okulewicz, 1987; Lewin, 1992a; Buchvarov, 2002b; reported as Rana agilis, Prokopic, Biserkov, 1995; Shimalov and Shimalov, 2000; Kirin, 1957 Rozman, 1976); Balkan stream frog, Rana graeca, 2002b); Natrix tessellata, (Sharpilo, 1976); European (Hristovski, 1974); European frog, Rana temporaria, catsnake, Telescopus fallax, (Sharpilo, 1976); Vipera (Baylis, 1928; Travassos, 1937; Ivanitzky, 1940; ammodytes, (Sharpilo, 1976); adder, Vipera berus, Kozlowska, 1960; Lees, 1962; Vojtková et al, 1963; (Moravec, 1963; Markov and Mozgovoi, 1969; Volna-Nabelkova, 1964; Kozák, 1969, 1973; Combes Moravec and Vojtková, 1975: Shimalov and Shimalov, et al., 1971; Hristovski and Lees, 1973; Frandsen, 1974; 2000; Novokhatskaya, 2008).

526 H. S. YILDIRIMHAN, C. R. BURSEY, F. N. ALTUNEL

Table. Helminths of Turkish lizards (1. Schad et al., 1960; 2. Tınar, 1982; 3. Tinar, 1983; 4. Saygı et al., 1993; 5. Yıldırımhan et al., 2006; 6. Yıldırımhan et al., 2008; 7. Yıldırımhan et al., 2009; 8. this paper. Anguis fragili Blanus strauchi turcicus Hemidactylus Lacerta parva Lacerta trilineata Lacerta viridis caucasia Laudakia Yauramia bkeyyio tauricus Podarcis

Lizard species Helminth

Digenea Plag iorchis elegans ------8 ------Pleurogenoides medians ------8 ------Brachylaemus sp. (metacercaria) ------8 ------Cestoda Oochoristica tuberculata ------8 --- 5 ------Joyeuxiella pasqualei ------3 ------Mesocestoides sp. (tetrathyridia) ------8 ------Nematoda Abbreviata abbreviata ------8 ------Ascrops strongylina (larva) ------8 ------Ascaridae (larva) ------5 --- Entomelas entomelas 1 ------Falcaustra armenica ------8 ------Foleyella candezei ------5 5 --- Oswaldocruzia fi liformis 1 ------1 ------1 Oxysomatium brevicaudatum 1 ------Parapharyngodon kasauli ------1 Parapharyngodon tyche ------5 5 --- Parapharyngodon micipsae --- 7 ------Physaloptera sp. (larva) ------1 ------Spauligodon cinsi ------4 ------Spauligodon laevicauda ------2,3,6 ------Skrjabinodon medinae ------8 ------Skrjabinelazia hoff manni ------8 ------Skrjabinelazia taurica ------1 Strongyluris calotis ------5 --- Th elandros baylisi ------5 ------Th elandros taylori ------5 --- Th elastomoides sp. --- 7 ------Acanthocephala Macracanthorhynchus catulinus ------6 ------

527 Helminth parasites of the Balkan green lizard, İ Bedriaga 1886, from Bursa, Turkey

Geographic range: Europe (Baker, 1987). Temporal distribution: 10 June 1996, 1 host with 8; Remarks: Lacerta trilineata represents a new host 4 May 1998, 2 hosts with 2, 5, respectively. record for O. fi liformis. Site of infection: Large intestine. Skrjabinelazia hoff manni Li, 1934 Type host and type locality: Lacerta muralis, Spain Prevalence and intensity: 1 of 38 (3%), 26. (García-Calvente, 1948) Temporal distribution: 24 June 1998, 1 host with Additional Turkish records: None. 26. Other reports: Reptilia: Podarcis muralis, (Dollfus et al., 1961; Hornero and Roca, 1992a); Lacerta Site of infection: Small intestine. schreiberi, (Roca and Ferragut, 1989); Podarcis Type host and type locality: Mongolia racerunner, bocagei, (Roca et al., 1989); Podaris hispanica, (Roca Eremias argus, China (Li, 1934). et al., 1986a; Roca and Lluch 1988; Roca et al., 1989; Additional Turkish records: None. Hornero and Roca, 1992a); Podarcis lilfordi, (Horneo and Roca, 1992b; Roca and Hornero, 1994); Podarcis Other reports: Reptilia: comb-toed gecko, pityusensis, (Hornero and Roca, 1992a; Roca and Crossobamon eversmanni, (Sharpilo, 1976); Kirghiz Hornero, 1994); Zootoca vivipara (reported as racerunner, Eremias nikolskii, (Sharpilo, 1976); Lacerta vivipara, Dollfus et al., 1961) Lacerta agilis, (Sharpilo, 1976; Sharpilo et al, 2001); Azarbaijan lizard, Darevskia raddei, reported as Geographic range: (Dollfus et al., 1961); Lacerta raddei, Khomustenko and Ataev, 1979); Spain (García-Calvente, 1948); Turkey (this report). Caucasian rock lizard, Darevskia saxicola, (reported Remarks: Lacerta trilineata represents a new host as Lacerta saxicola, Sharpilo, 1976); Lacerta viridis, record for S. medinae; Turkey is a new locality record. (Biserkov and Kostadinova, 1998); Podarcis bocagei, (Galdón et al., 2006); Carbonell’s wall lizard, Podarcis carbonelli (Galdón et al., 2006); Podarcis lilfordi, Discussion (Hornero and Roca, 1992b; Roca and Hornero, Sixteen (42%) of 38 Lacerta trilineata harbored 1994); Podarcis muralis, (Kirin, 2002a); Tarentola 217 helminths representing 11 species: 12 lizards angustimentalis, (Roca et al., 1990); Teratoscincus harbored 1 species, 3 lizards harbored 2 species, scincus, (Sharpilo, 1976). and 1 harbored 4 species. Th ere were 13.6 ± 25.5 SD Geographic range: Azerbaijan (Khomustenko and helminth individuals per infected host and 1.4 ± 0.8 Ataev, 1979); Bulgaria (Biserkov and Kostadinova, helminth species per infected host. 1998); Central Asia (Sharpilo, 1976); China (Li, To our knowledge, helminth lists are available for 1934); Portugal (Galdón et al., 2006); Spain (Hornero 5 species of Turkish lizards, Anguis fragilis, Blanus and Roca, 1992b); Turkey (this report). strauchi, Hemidactylus turcicus, Lacerta parva, Lacerta viridis, Laudakia caucasia, Laudakia stellio, Remarks: Lacerta trilineata represents a new host and (Schad et al., 1960; Tınar, 1982, record for S. hoff manni; Turkey is a new locality 1983; Yıldırımhan et al., 2006, 2008, 2009). Th is record. report presents an initial helminth list for the ninth Skrjabinodon medinae species. Baran and Atatür (1998) identify 53 species (García-Calvente, 1948) Specian and Ubelaker, known to occur in Turkey; thus, additional studies 1974 will be required before the component community of helminths infecting Turkish lizards can be (Syn. Pharyngodon medinae García-Calvente determined. Currently, we can say that Turkish lizards 1948; Parathelandros medinae [García-Calvente, are infected by generalist nematodes, i.e. nematode 1948] Read and Amrein, 1953). species that infect more than one host species. A Prevalence, mean intensity, and range: 3 of 38 summary of known Turkish lizard helminths is (8%), 5.0 ± 3.0, 2-8. presented in the Table.

528 H. S. YILDIRIMHAN, C. R. BURSEY, F. N. ALTUNEL

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